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Infection by the Castrating Parasitic Nematode Sphaerularia Bombi Changes Gene Expression in Bombus Terrestris Bumblebee Queens

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Infection by the Castrating Parasitic Nematode Sphaerularia Bombi Changes Gene Expression in Bombus Terrestris Bumblebee Queens Infection by the castrating parasitic nematode Sphaerularia bombi changes gene expression in Bombus terrestris bumblebee queens Thomas J. Colgan1,2,3*, James C. Carolan4, Seirian Sumner5, Mark L. Blaxter6, Mark J. F. Brown7* Affiliation: 1. Department of Zoology, School of Natural Sciences, University of Dublin, Trinity College, Dublin 2, Ireland. 2. School of Biological and Chemical Sciences, Queen Mary University of London, London, E1 4NS, United Kingdom. 3. School of Biological, Earth and Environmental Sciences, University College Cork, Cork, Ireland. 4. Department of Biology, Maynooth University, Maynooth, County Kildare, Ireland. 5. Centre for Biodiversity and Environment Research, University College London, Gower Street, London WC1E 6BT, United Kingdom. 6. School of Biological Sciences, Institute of Evolutionary Biology, University of Edinburgh, Edinburgh, EH9 3JT, United Kingdom. 7. Department of Biological Sciences, Centre for Ecology, Evolution and Behaviour, Royal Holloway University of London, Egham Hill, Egham, TW20 0EX, United Kingdom. Correspondence: Thomas J. Colgan [email protected] Mark J.F. Brown [email protected] Short running title: Nematode alters bumblebee queen gene expression. 1 Abstract Parasitism can result in dramatic changes in host phenotype, which are themselves underpinned by genes and their expression. Understanding how hosts respond at the molecular level to parasites can therefore reveal the molecular architecture of an altered host phenotype. The entomoparasitic nematode Sphaerularia bombi is a parasite of bumblebee (Bombus) hosts where it induces complex behavioural changes and host castration. To examine this interaction at the molecular level, we performed genome-wide transcriptional profiling using RNA-Seq of S. bombi-infected Bombus terrestris queens at two critical time-points: during and just after overwintering diapause. We found that infection by S. bombi affects the transcription of genes underlying host biological processes associated with energy usage, translation, and circadian rhythm. We also found that the parasite affects the expression of immune genes, including members of the Toll signaling pathway providing evidence for a novel interaction between the parasite and the host immune response. Taken together, our results identify host biological processes and genes affected by an entomoparasitic nematode providing the first steps towards a molecular understanding of this ecologically important host-parasite interaction. Keywords: pollinator health, insect immunity, molecular parasitism, extended phenotype. 2 Introduction Host-parasite interactions are amongst the most complex in the biological world (Poulin 1995). Both host and parasite can exert enormous selective pressures upon the other, and these have shaped their individual and co-evolutionary trajectories (Combes 2001). Central to this process is the genome, and the products it encodes for. Whilst the characterisation of selection signatures within host and parasite genomes can provide an insight into the evolutionary relationship between them (Combes 2001), investigating the expression of the genomes can identify the genes and genetic systems involved in these dynamic interactions (Biron & Loxdale 2013). Parasitism can result in dramatic changes in the host phenotype, which may be a direct or indirect consequence of the host-parasite interaction. The expression of parasite genes can directly modify their hosts, resulting in an “extended phenotype” (Dawkins 1982). For example, parasites of humans secrete molecules that manipulate aspects of the host immune system (Maizels & Yazdanbakhsh 2003; Hewitson et al. 2009; McSorley et al. 2013; Buck et al. 2014), in some cases through effector proteins that have evolved to mimic or alter host functions (Sacks & Sher 2002). Dramatic examples of parasite-determined host phenotypes are also evident in insect hosts. Proteomic profiling identified candidate grasshopper host proteins with roles in neurogenesis that were impacted by infection with the nematomorph, Spinochordodes tellinii (Biron et al. 2005), and induced hydrophilic behaviour to enable completion of the parasite lifecycle, which resulted in host death through drowning (Thomas et al. 2002). High throughput transcriptomics has similarly uncovered genes underlying complex altered host phenotypes in response to parasite infections (de Bekker et al. 2015; Geffre et al. 2017; Guo et al. 2017). 3 Altered host phenotypes may be an indirect response to infection or present a parasite adaptation to increase parasite fitness. The entomoparasitic nematode, Sphaerularia bombi (Fig. 1B), infects and castrates queens in multiple species of bumblebee (Bombus) (Fig. 1A); it is found throughout the northern hemisphere (Khan 1957; Alford 1969a; McCorquodale et al. 1998; Rutrecht & Brown 2008; Maxfield-Taylor et al. 2011), South America (Plischuk & Lange 2012), and has been introduced to New Zealand (Macfarlane & Griffin 1990). S. bombi infection induces complex changes in the host phenotype, which have been suggested to increase parasite transmission (Poinar & Van Der Laan 1972; Lundberg & Svensson 1975). Infection of Bombus queens occurs in overwintering sites during host diapause (Pouvreau 1962; Madel 1966; Poinar & Van Der Laan 1972)(Fig. 1C). The exact site of host entry is unknown but the infective female adult stage is suggested to be able to enter through the mouth, anus or between the tegumental plates of the host (Poinar & Van Der Laan 1972). Upon entry, the nematode migrates to the host haemocoel and begins to evert its uterus and associated reproductive tract (Poinar & Van Der Laan 1972). Eversion is paused and the nematode enters a dormant state, overwintering within the diapausing host. When the infected host emerges from diapause, the nematode resumes eversion of its reproductive tract, which expands to a volume 300 times larger than that of the nematodes’ body size. The nematode absorbs nutrients directly from the host haemolymph via invaginations present on the everted uterus (Poinar & Hess 1972). Eggs, containing larval stage 1 (L1) juveniles, are released into the haemocoel of the host, which undergo two further moults before emerging as stage 3 larvae (L3). L3 juveniles remain within the host for a period of time before actively burrowing into the digestive tract and exiting via the anus. L3 juveniles enter the soil and undergo two further moults before reaching sexual maturity. Females are fertilised and reside in the soil until contact with new hosts (Madel 1966; Poinar & Van Der Laan 1972). 4 Parasitised queens display altered behaviour compared to uninfected queens. Post-diapause, uninfected queens forage for resources before locating a nesting site and establishing a colony (Alford 1975) (Fig. 1). In comparison, parasitised queens forage but do not establish a colony, instead they investigate prospective overwintering sites, where parasite offspring are actively deposited (Poinar & Van Der Laan 1972; Lundberg & Svensson 1975). This behaviour coincides with a lack of development of the corpora allata (Palm 1948; Röseler & Röseler 1973; Röseler 2002), an endocrine organ that develops in uninfected queens post-diapause to produce juvenile hormone, a key regulator of ovarian development. This restriction has been suggested to be caused by secretions released by the parasite (Palm 1948; Pouvreau 1962) although examination and characterisation of secretory molecules by S. bombi has not yet been performed. Such morphological and behavioural changes are thought to represent a parasite adaptation that facilitates the dispersal of parasite progeny across locations to increase the probability of novel host encounter (Lundberg & Svensson 1975). In addition to the direct effects of S. bombi on bumblebee queens, the nematode can have indirect ecological effects through the displacement of uninfected workers at foraging sites by S. bombi-infected queens (Kadoya & Ishii 2015). Given that parasite prevalence can be as high as 50% within certain geographical regions (Kelly 2009), the nematode may also impact host population dynamics. Consequently, understanding the interaction between S. bombi and its bumblebee hosts may help us elucidate drivers of host population dynamics in these globally declining pollinators (Brown & Paxton 2009). Functional genomic techniques, such as RNA-Seq, provide an unbiased view into genome-wide transcriptional changes and have been applied to macroparasite-insect systems to elucidate genes underlying complex altered host phenotypes (Choi et al. 2014; Geffre et al. 2017). For the bumblebee, recent developments in genomics and transcriptomics have provided the tools to 5 explore important aspects of host biology, including phenotypic polymorphism (Colgan et al. 2011; Harrison et al. 2015), caste differentiation (Woodard et al. 2014; Collins et al. 2017), mating success (Manfredini et al. 2017) and diapause regulation (Amsalem et al. 2015a). In relation to pathogen response, previous transcriptomic studies have identified changes in host immune expression in response to the trypanosomatid Crithidia bombi (Barribeau et al. 2014) and bacterial challenge (Barribeau et al. 2016). However, investigation of changes in host gene expression in response to a macroparasite such as S. bombi has not been reported. Here we conduct a quantitative transcriptomic analysis using RNA-Seq to identify changes within the host transcriptome in response to S. bombi infection at two critical time-points: during diapause,
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